Making starch

Current Opinion in Plant Biology

Volumn 2, Issue 3, 1999, Pages 223-229

  Smith, Alison M ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0033152252     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5266(99)80039-9     Document Type: Article

References (48)

1. Heyer AG, Lloyd JR, Kossmann J: Production of modified polymeric carbohydrates. Curr Opin Biotech 1999, 10:in press.
2. Jenkins PJ, Cameron RE, Donald AM: A universal feature in the structure of starch granules from different botanical sources. Starch 1993, 45:417-420.
3. Gallant DJ, Bouchet B, Baldwin PM: Microscopy of starch: Evidence of a new level of granule organization. Carbohydr Polym 1997, 32:177-191.
4. Oostergetel GT, Van Bruggen EJF: The crystalline domains in potato starch granules are arranged in a helical fashion. Carbohydr Polym 1993, 21:7-12.
5. Bogracheva TY, Morris VJ, Ring SG, Hedley CL: The granular structure of C-type pea starch and its role in gelatinization. Biopolymers 1998, 45:323-332. References [5•] and [6•] use sophisticated techniques to explore the internal structure of starch granules from pea embryos. These granules are known to contain two different sorts of amylopectin crystallites, A and B (hence the term C-type starch), which reflect two different types of packing of the double helices within clusters (see Figure 1 above). Whether A or B crystallites are formed is thought to be related to the average chain lengths of chains within amylopectin clusters: A crystallites are formed from shorter and B crystallites from longer chains. Both studies report that the inner part of the pea starch granule is enriched in B and the outer part in A crystallites. The implication is that chain lengths of amylopectin in the inner and outer part of the granule are different. This difference could result from the changes during embryo development in relative activities of different isoforms of starch synthase and SBE [13], and also from modification of amylopectin within the granule matrix (see [38] and discussion of [24••]). Although pea starch is unusual in containing both A and B crystallites, there is also evidence from potato of differences in polymer structure and composition between the core and the periphery of the granule [7]. The pea may be a good system in which to explore the origins of such differences.
6. Buléon A, Gérard C, Riekel C, Vuong R, Chanzy H: Details of the crystalline ultrastructure of C-starch granules revealed by syntchrotron microfocus mapping. Macromol 1998, 31:6605-6610. See annotation for [5•].
7. Jane J, Shen JJ: Internal structure of the potato starch granule revealed by chemical gelatinization. Carbohydr Res 1993, 247:279-290.
8. Waigh TA, Perry P, Riekel C, Gidley MJ, Donald AM: Chiral side-chain liquid-crystalline polymeric properties of starch. Macromolecules 1998, 22:7980-7984. Donald and colleagues suggest that the structure of amylopectin is consistent with that of a side-chain liquid-crystal polymer. They point out that several important physical properties of starch can be explained on this basis. The suggestion would also legitimise the belief that physical rather than biological processes promote the organisation of newly-synthesised amylopectin at the granule surface. The full implications of this suggestion for the mechanism of synthesis of the granule have yet to be explored, but they may be considerable.
9. Wong KS, Jane J: Quantitative analysis of debranched amylopectin by HPAEC-PAD with a postcolumn enzyme reactor. J Liq Chrom Rel Technol 1997, 20:297-310.
10. Morell MK, Samuel MS, O'Shea MG: Analysis of starch structure using fluorophore-assisted carbohydrate electrophoresis. Electrophoresis 1998, 19:2603-2611. New methods for the separation and quantification of chains of amylopectin are described. Amylopectin is debranched with isoamylase, and chains are tagged with a fluorophore. Chains are then separated and quantified by gel or capillary electrophoresis coupled with fluorescence detection. The gel electrophoresis method uses a standard Applied Biosystems DNA sequencer and software. It has several potential advantages over the widely-used method involving anion-exchange chromatography coupled with pulsed amperometric detection. For example many samples can be analysed simultaneously, allowing a high level of replication and hence statistical analysis of differences between samples. This method is used in the work described in [12••].
11. McPherson AE, Jane J: Physicochemical properties of selected root and tuber starches. Carbohydr Polym 1999, in press.
12. Edwards A, Fulton DC, Hylton CM, Jobling SA, Gidley M, Rössner U, Martin C, Smith AM: A combined reduction in activity of starch synthases II and III of potato has novel effects on the starch of tubers. Plant J 1999, 17:251-261. The studies in [12••] and [28••] describe the structure and properties of amylopectin in tubers of transgenic potato plants with reduced activities of either the SSII or the SSIII isoform of starch synthase or of both isoforms together. Comparison of results from the three sorts of plant reveals that the effect upon amylopectin of reduction of a particular isoform depends upon the level of activity of the other isoform. This apparent synergy between the actions of the two isoforms is explained in terms of the complexity of the substrate presented to an isoform of starch synthase in vivo. The structure of the substrate, and hence the contribution of the isoform to its synthesis, will depend upon other starch synthesising and modifying enzymes present in the amyloplast, and this in turn will depend upon a host of genetic, environmental and developmental factors. The role of an isoform in vivo is thus determined in part by its intrinsic properties, and in part by the background in which it is being expressed. This is perhaps bad news for the cause of rational manipulation of starch structure, but at least it implies that almost any manipulation of combinations of starch synthesising enzyme may have surprising and potentially useful results. The two papers are also good illustrations of the use of chimeric constructs to express two antisense RNAs simultaneously.
13. Burton RA, Bewley JD, Smith AM, Bhattacharyya MK, Tatge H, Ring S, Bull V, Hamilton WDO, Martin C: Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J 1995, 7:3-17.
14. Morell MK, Blennow A, Kosar-Hashemi B, Samuel MS: Differential expression and properties of starch branching enzyme isoforms in developing wheat endosperm. Plant Physiol 1997, 113:201-208.
15. Kuriki T, Stewart DC, Preiss J: Construction of chimeric enzymes out of maize endosperm branching enzymes I and II: Activity and properties. J Biol Chem 1997, 46:28999-29004.
16. Tomlinson KL, Lloyd JR, Smith AM: Importance of isoforms of starch-branching enzyme in determining the structure of starch in pea leaves. Plant J 1997, 11:31-43.
17. Edwards A, Marshall J, Sidebottom C, Visser RGF, Smith AM, Martin C: Biochemical and molecular characterisation of a novel starch synthase from potato tubers. Plant J 1995, 8:283-294.
18. Marshall J, Sidebottom C, Debet M, Martin C, Smith AM, Edwards A: Identification of the major starch synthase in the soluble fraction of potato tubers. Plant Cell 1996, 8:1121-1135.
19. Abel GJW, Springer F, Willmitzer L, Kossmann J: Cloning and functional analysis of a cDNA encoding a novel 139 kDa starch synthase from potato (Solanum tuberosum L.). Plant J 1996, 10:981-991.
20. Kossmann J, Abel GJW, Springer F, Lloyd JR, Willmitzer L: Cloning and functional analysis of a cDNA encoding a starch synthase from potato (Solanum tuberosum L.) that is predominantly expressed in leaf tissue. Planta 1999, in press.
21. Knight ME, Harn C, Lilley CER, Guan HP, Singletary GW, Mu-Forster C, Wasserman BP, Keeling PL: Molecular cloning of starch synthase I from maize (W64) endosperm and expression in Escherichia coli. Plant J 1998, 14:613-622. [21•,22•,23••] describe the identification at a molecular level of the three isoforms of starch synthase likely to account for the amylopectin-synthesising activity of the maize endosperm. This paper describes an isoform of the SSI class first identified in rice [26] and recently found in potato, where it is expressed primarily in leaves [20].
22. Harn C, Knight M, Ramakrishnan A, Guan HP, Keeling PL, Wasserman PL: Isolation and characterization of the zSSIIa and zSSIIb starch synthase clones from maize endosperm. Plant Mol Biol 1998, 37:639-649. See annotation for [21•]. Here cDNAs encoding two isoforms of the SSII class are described, only one of which (zSSIIa) is abundant in the endosperm. The zSSIIa gene is reported to map approximately to the sugary2 (su2) locus, raising the possibility that loss of this isoform is the primary cause of the alterations in amylopectin structure seen in su2 mutants. The rug5 mutant of pea described in [24••] also lacks an isoform of the SSII class.
23. Gao M, Wanat J, Stinard PS, James MG, Myers AM: Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 1998, 10:399-412. See annotation for [21•]. The gene at the Dull1 locus of maize is shown to encode a starch synthase. The protein is more similar to the SSIII isoform of potato than to isoforms of the SSII and SSI classes, but a large amino-terminal portion of the protein is substantially different in sequence from any previously described isoforms. dull1 mutations bring about large changes in the structure of amylopectin, hence this discovery provides further evidence that individual isoforms of starch synthase play specific roles in amylopectin synthesis. The precise contribution of the DU1 starch synthase is difficult to deduce because the mutation has pleiotropic effects on other enzymes of starch synthesis (see [27]). The authors suggest that at least some of these effects may be the consequence of destabilisation of a putative starch-synthesising complex of which the DU1 starch synthase is a component. They point out features of the amino-terminal region of the DU1 protein which might be involved in protein-protein interactions with SBE. This intriguing idea remains to be rigorously tested.
24. Craig J, Lloyd JR, Tomlinson K, Barber L, Edwards A, Wang TL, Martin C, Hedley CL, Smith AM: Mutations in the gene encoding starch synthase II profoundly alter amylopectin structure in pea embryos. Plant Cell 1998, 10:413-426. Mutations at the rug5 locus of pea are shown to lie in the gene encoding SSII, the isoform of starch synthase responsible for about 60% of the amylopectin-synthesising activity of the developing embryo. Although the mutations have little effect on the rate of starch synthesis during most of embryo development, they cause a decrease in amylopectin chains of intermediate length, thought to span two clusters (see Figure 1), and an increase in the very short chains. This indicates that SSII plays a specific role in the synthesis of chains of intermediate length in the wild-type embryo. There is also an increase in very long chains of amylopectin. It is suggested that this may be attributable to an increased specific activity of GBSSI in the mutant. This is consistent with a growing body of evidence, not discussed in this review, that GBSSI is not only responsible for amylose synthesis but also contributes to the synthesis of long chains in the amylopectin fraction of the granule matrix (see [39,40••]).
25. Munyikawa TRI, Langeveld S, Salehuzzaman SNIM, Jacobsen E, Visser RGF: Cassava starch biosynthesis: New avenues for modifying starch quantity and quality. Euphytica 1997, 96:65-75.
26. Baba T, Nishihara M, Mizuno K, Kawasaki T, Shimada H, Kobayashi E, Ohnishi S, Tanaka K, Arai Y: Identification, cDNA cloning, and gene expression of soluble starch synthase in rice (Oryza sativa L.) immature seeds. Plant Physiol 1993, 103:565-573.
27. Singletary GW, Banisadr R, Keeling P: Influence of gene dosage on carbohydrate synthesis and enzyme activities in endosperm of starch-deficient mutants of maize. Plant Physiol 1997, 113:291-304.
28. Lloyd JR, Landschütze V, Kossmann J: Simultaneous antisense inhibition of two starch synthase isoforms in potato tubers leads to accumulation of grossly modified amylopectin. Biochem J 1999, 338:515-521. See annotation for [12••].
29. Ball S, Guan HP, James M, Myers A, Keeling P, Mouille G, Buljon A, Colonna P, Preiss J: From glycogen to amylopectin: A model for the biogenesis of the starch granule. Cell 1996, 86:349-352.
30. Doehlert DC, Kuo TM, Juvik JA, Beers EP, Duke SH: Characteristics of carbohydrate metabolism in sweet corn (sugary-1) endosperms. J Am Soc Hort Sci 1993, 118:661-666.
31. James MG, Robertson DS, Myers AM: Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 1995, 7:417-429.
32. Nakamura Y, Umemoto T, Takahata Y, Komae K, Amano E, Satoh H: Changes in structure of starch and enzyme activities affected by sugary mutations in developing rice endosperm: Possible role of starch debranching enzyme (R-enzyme) in amylopectin synthesis. Physiol Plant 1996, 97:491-498.
33. Nakamura Y, Kubo A, Shimamune T, Matsuda T, Harada K, Satoh H: Correlation between activities of starch debranching enzyme and α-polyglucan structure in endosperms of sugary-1 mutants of rice. Plant J 1997, 12:143-153.
34. Mouille G, Maddelein ML, Libessart N, Tagala P, Decq A, Delrue B, Ball S: Preamylopectin processing: A mandatory step for starch biosynthesis in plants. Plant Cell 1996, 8:1353-1366.
35. Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, Smith AM, Chen J: A mutant of Arabidopsis lacking chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 1998, 10:1699-1711. A mutant of Arabidopsis is shown to accumulate most of its glucan as phytoglycogen rather than starch, and to lack a DBE of the isoamylase class. It is, therefore, comparable with the su1 mutants of cereals and the sta7 mutant of Chlamydomonas, described in [30-34]. Detailed analysis shows that individual chloroplasts accumulate simultaneously both phytoglycogen and starch granules containing amylopectin very similar to that in wild-type leaves. The authors explain this phenotype by proposing that DBE is one of a suite of enzymes required to prevent the production of highly-branched soluble glucans from malto-oligosaccharides at the expense of amylopectin synthesis at the granule surface. This proposal for the role of DBE in starch sythesis differs radically from that put forward in [29]. Neither of these proposals has yet been rigorously tested.
36. Zhu ZP, Hylton CM, Rössner U, Smith AM: Characterization of starch-debranching enzymes in pea embryos. Plant Physiol 1998, 118:581-590.
37. Martin C, Smith AM: Starch biosynthesis. Plant Cell 1995, 7:971-985.
38. Tatge H, Marshall J, Martin C, Edwards EA, Smith AM: Evidence that amylose synthesis occurs within the matrix of the starch granule in potato tubers. Plant Cell Env 1999, in press.
39. Denyer K, Clarke B, Hylton C, Smith AM: The elongation of amylose and amylopectin chains in isolated starch granules. Plant J 1996, 10:1135-1143.
40. Van de Wal M, D'Hulst C, Vincken JP, Buléon A, Visser R, Ball S: Amylose is synthesized in vitro by extension of and cleavage from amylopectin. J Biol Chem 1998, 272:22232-22240. Using starch granules isolated from the unicellular alga Chlamydomonas, the authors show that amylopectin within the granule matrix can act as a substrate for amylose synthesis via the granule-bound starch synthase. During prolonged incubations of the granules, long chains which have been elongated by the granule-bound enzyme are cleaved from amylopectin within the matrix to produce amylose. The mechanism of cleavage is presently unknown. Models are proposed in which the cleavage occurs via either the granule-bound enzyme itself, utilising a putative hydrolytic domain, or the chain-transfer reaction catalysed by a granule-bound starch-branching enzyme. The authors suggest that this amylopectin-based mechanism is a more likely route of amylose synthesis in Chlamydomonas than elongation of soluble malto-oligosaccharides shown to give rise to amylose in isolated granules from pea, potato [39] and Chlamydomonas (this reference). Neither of these routes has yet been shown to operate in vivo.
41. Buttrose MS: Submicroscopic development and structure of starch granule in cereal endosperms. J Ultrastruc Res 1960, 4:231-257.
42. Blennow A, Bay-Smidt AM, Wischmann B, Olsen CE, Møller BL: The degree of starch phosphorylation is related to the chain length distribution of the neutral and the phosphorylated chains of amylopectin. Carbohydr Res 1998, 307:45-54. References [42•] and [43•] enforce the idea that the phosphorylation of amylopectin occurs via a common mechanism during the synthesis of amylopectin in a very wide range of species, and that the mechanism of phosphorylation is intimately related to the process of amylopectin synthesis. Here, a detailed analysis of phosphorylated chains in starches from several species reveals a strong relationship between the chain length profile of amylopectin and the degree of phosphorylation.
43. Wischmann B, Nielsen TH, Møller BL: In vitro biosynthesis of phosphorylated starch in intact potato amyloplasts. Plant Physiol 1999, 119:1-8 See annotation for [42•]. Supply of radiolabelled glucose 6-phosphate to amyloplasts isolated from potato tubers reveals that the phosphate group of the hexose phosphate is incorporated into amylopectin. This may provide a valuable system on which to study the mechanism of phosphorylation.
44. Lorberth R, Ritte G, Willmitzer L, Kossmann J: Inhibition of a starch granule-bound protein leads to modified starch and repression of cold sweetening. Nat Biotechnol 1998, 16:473-477. Levels of a 155-kD protein found in the starch granules of potatoes are reported to influence both the level of phosphorylation of starch and the extent of its degradability. Reduction in levels of the protein (termed R1) throughout the plant by expression of antisense RNA resulted in a large decrease in the phosphorylation of tuber starch. The level of starch in leaves was higher than that in control plants, and net starch degradation in stored tubers was reduced. The relationship between the apparently reduced rate of degradation of starch and the reduction in its phosphorylation are not understood, and the predicted amino-acid sequence of the R1 protein does not reveal its likely function. Expression of the gene in E. coli, however, led to a greater degree of phosphorylation of the bacterial glycogen, suggesting that R1 is directly involved in the phosphorylation of glucan chains. DNA sequences similar to that of the R1 gene have been reported from rice and Arabidopsis.
45. Takaha T, Critchley J, Okada S, Smith SM: Normal starch content and composition in tubers of antisense potato plants lacking D-enzyme (4-α-glucanotransferase). Planta 1998, 205:445-451.
46. Albrecht T, Burkhard G, Pusch K, Kossmann J, Buchner P, Wobus U, Steup M: Homodimers and heterodimers of Pho1-type phosphorylase isoforms in Solanum tuberosum L. as revealed by sequence-specific antibodies. Eur J Biochem 1998, 251:343-352.
47. Smythe C, Cohen P: The discovery of glycogenin and the priming mechanism for glycogenesis. Eur J Biochem 1991, 200:625-632.
48. Bocca SN, Rothschild A, Tandecarz JS: Initiation of starch biosynthesis: Purification and characterization of UDP-glucose:Protein transglucosylase from potato tubers. Plant Physiol Biochem 1997, 35:205-212.